Crystallographic analysis and structure-guided engineering of NADPH-dependent ralstonia sp. alcohol dehydrogenase toward NADH cosubstrate specificity

Biotechnology and Bioengineering

Volumn 110, Issue 11, 2013, Pages 2803-2814

  Lerchner, Alexandra ^a   Jarasch, Alexander ^a   Meining, Winfried ^a   Schiefner, André ^a   Skerra, Arne ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

Enzymology; Protein crystallography; Protein engineering; RasADH; Rossmann fold

Indexed keywords

ENZYMOLOGY; PROTEIN CRYSTALLOGRAPHY; PROTEIN ENGINEERING; RASADH; ROSSMANN FOLD;

AMINO ACIDS; ETHANOL; KETONES; PROTEINS; SUBSTRATES;

ENZYMES;

ALCOHOL DEHYDROGENASE; ALCOHOL DERIVATIVE; AMINO ACID; DINUCLEOTIDE; HOMODIMER; KETONE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; OXIDOREDUCTASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE;

ARTICLE; BIOCATALYST; BIOTECHNOLOGY; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; ENZYME KINETICS; ENZYME SPECIFICITY; ENZYMOLOGY; INFORMATION; NONHUMAN; PROTEIN DOMAIN; PROTEIN MOTIF; RALSTONIA; STEREOCHEMISTRY;

RALSTONIA SP.;

ENZYMOLOGY; PROTEIN CRYSTALLOGRAPHY; PROTEIN ENGINEERING; RASADH; ROSSMANN FOLD;

ALCOHOL OXIDOREDUCTASES; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; COENZYMES; CRYSTALLOGRAPHY, X-RAY; DNA MUTATIONAL ANALYSIS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; NAD; NADP; PROTEIN CONFORMATION; PROTEIN ENGINEERING; PROTEIN MULTIMERIZATION; RALSTONIA; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT; SUBSTRATE SPECIFICITY;

EID: 84884533760     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.24956     Document Type: Article

References (52)

1. Benach J, Atrian S, Gonzalez-Duarte R, Ladenstein R. 1999. The catalytic reaction and inhibition mechanism of Drosophila alcohol dehydrogenase: Observation of an enzyme-bound NAD-ketone adduct at 1.4 Å resolution by X-ray crystallography. J Mol Biol 289:335-355.
2. Berenguer-Murcia A, Fernandez-Lafuente R. 2010. New trends in the recycling of NAD(P)H for the design of sustainable asymmetric reductions catalyzed by dehydrogenases. Curr Org Chem 14:1000-1021.
3. Biegert A, Mayer C, Remmert M, Söding J, Lupas AN. 2006. The MPI Bioinformatics Toolkit for protein sequence analysis. Nucleic Acids Res 34:W335-W339.
4. Bond CS, Schüttelkopf AW. 2009. ALINE: A WYSIWYG protein-sequence alignment editor for publication-quality alignments. Acta Crystallogr D Biol Crystallogr 65:510-512.
5. Chen R, Greer A, Dean AM. 1995. A highly active decarboxylating dehydrogenase with rationally inverted coenzyme specificity. Proc Natl Acad Sci USA 92:11666-11670.
6. +-dependent 15-hydroxyprostaglandin dehydrogenase. Arch Biochem Biophys 419:139-146.
7. Cuetos A, Rioz-Martínez A, Bisogno FR, Grischek B, Lavandera I, de Gonzalo G, Kroutil W, Gotor V. 2012. Access to enantiopure α-alkyl-β-hydroxy esters through dynamic kinetic resolutions employing purified/overexpressed alcohol dehydrogenases. Adv Synth Catal 354:1743-1749.
8. Davis IW, Leaver-Fay A, Chen VB, Block JN, Kapral GJ, Wang X, Murray LW, Arendall WB III, Snoeyink J, Richardson JS, Richardson DS. 2007. MolProbity: All-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res 35:W375-W383.
9. Ehrensberger AH, Elling RA, Wilson DK. 2006. Structure-guided engineering of xylitol dehydrogenase cosubstrate specificity. Structure 14:567-575.
10. M: A useful comparator? Trends Biotechnol 25:247-249.
11. Emsley P, Lohkamp B, Scott WG, Cowtan K. 2010. Features and development of COOT. Acta Crystallogr D Biol Crystallogr 66:486-501.
12. Ferreira-Silva B, Lavandera I, Kern A, Faber K, Kroutil W. 2010. Chemo-promiscuity of alcohol dehydrogenases: Reduction of phenylacetaldoxime to the alcohol. Tetrahedron 66:3410-3414.
13. Filling C, Nordling E, Benach J, Berndt KD, Ladenstein R, Jörnvall H, Oppermann U. 2001. Structural role of conserved Asn179 in the short-chain dehydrogenase/reductase scaffold. Biochem Biophys Res Commun 289:712-717.
14. Filling C, Berndt KD, Benach J, Knapp S, Prozorovski T, Nordling E, Ladenstein R, Jörnvall H, Oppermann U. 2002. Critical residues for structure and catalysis in short-chain dehydrogenases/reductases. J Biol Chem 277:25677-25684.
15. Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appel RD, Bairoch A. 2005. Protein identification and analysis tools on the ExPASy server. In: Walker JM, editor. The proteomics protocols handbook. New York, NY: Humana Press. p 571-607.
16. Jörnvall H, Danielsson O, Hjelmqvist L, Persson B, Shafqat J. 1995a. The alcohol dehydrogenase system. Adv Exp Med Biol 372:281-294.
17. Jörnvall H, Persson B, Krook M, Atrian S, Gonzalez-Duarte R, Jeffery J, Ghosh D. 1995b. Short-chain dehydrogenases/reductases (SDR). Biochemistry 34:6003-6013.
18. Kabsch W. 2010. XDS. Acta Crystallogr D Biol Crystallogr 66:125-132.
19. Kabsch W, Sander C. 1983. Dictionary of protein secondary structure: Pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22:2577-2637.
20. Kavanagh KL, Jörnvall H, Persson B, Oppermann U. 2008. The SDR superfamily: Functional and structural diversity within a family of metabolic and regulatory enzymes. Cell Mol Life Sci 65:3895-3906.
21. Khoury GA, Fazelinia H, Chin JW, Pantazes RJ, Cirino PC, Maranas CD. 2009. Computational design of Candida boidinii xylose reductase for altered cofactor specificity. Protein Sci 18:2125-2138.
22. + ribose OH switch. Proteins 51:289-298.
23. Kulig J, Simon RC, Rose CA, Husain SM, Häckh M, Lüdeke S, Zeitler K, Kroutil W, Pohl M, Rother D. 2012. Stereoselective synthesis of bulky 1, 2-diols with alcohol dehydrogenases. Catal Sci Technol 2:1580-1589.
24. Lavandera I, Kern A, Ferreira-Silva B, Glieder A, de Wildeman S, Kroutil W. 2008. Stereoselective bioreduction of bulky-bulky ketones by a novel ADH from Ralstonia sp. J Org Chem 73:6003-6005.
25. Liese A, Seelbach K, Wandrey C. 2006. Industrial biotransformations. Weinheim: Wiley-VCH.
26. Liu W, Wang P. 2007. Cofactor regeneration for sustainable enzymatic biosynthesis. Biotechnol Adv 25:369-384.
27. + reductase by site-directed mutagenesis. J Biol Chem 276:11902-11912.
28. Michaelis L, Menten ML, Johnson KA, Goody RS. 2011. The original Michaelis constant: Translation of the 1913 Michaelis-Menten paper. Biochemistry 50:8264-8269.
29. Mueller U, Darowski N, Fuchs MR, Forster R, Hellmig M, Paithankar KS, Puhringer S, Steffien M, Zocher G, Weiss MS. 2012. Facilities for macromolecular crystallography at the Helmholtz-Zentrum Berlin. J Synchrotron Radiat 19:442-449.
30. Murshudov GN, Skubak P, Lebedev AA, Pannu NS, Steiner RA, Nicholls RA, Winn MD, Long F, Vagin AA. 2011. REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr D Biol Crystallogr 67:355-367.
31. Musa MM, Phillips RS. 2011. Recent advances in alcohol dehydrogenase-catalyzed asymmetric production of hydrophobic alcohols. Catal Sci Technol 1:1311-1323.
32. Oppermann UC, Filling C, Berndt KD, Persson B, Benach J, Ladenstein R, Jörnvall H. 1997. Active site directed mutagenesis of 3β/17β-hydroxysteroid dehydrogenase establishes differential effects on short-chain dehydrogenase/reductase reactions. Biochemistry 36:34-40.
33. Oppermann U, Filling C, Hult M, Shafqat N, Wu X, Lindh M, Shafqat J, Nordling E, Kallberg Y, Persson B, Jörnvall H. 2003. Short-chain dehydrogenases/reductases (SDR): The 2002 update. Chem Biol Interact 143-144:247-253.
34. Painter J, Merritt EA. 2006. TLSMD web server for the generation of multi-group TLS models. J Appl Cryst 39:109-111.
35. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE. 2004. UCSF chimera-A visualization system for exploratory research and analysis. J Comput Chem 25:1605-1612.
36. Ploux O, Lei Y, Vatanen K, Liu HW. 1995. Mechanistic studies on CDP-6-deoxy-delta 3, 4-glucoseen reductase: The role of cysteine residues in catalysis as probed by chemical modification and site-directed mutagenesis. Biochemistry 34:4159-4168.
37. Rossmann MG, Moras D, Olsen KW. 1974. Chemical and biological evolution of nucleotide-binding protein. Nature 250:194-199.
38. Sambrook J, Fritsch, EF, Maniatis, T. 2001. Molecular cloning: A laboratory manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
39. Scrutton NS, Berry A, Perham RN. 1990. Redesign of the coenzyme specificity of a dehydrogenase by protein engineering. Nature 343:38-43.
40. Skerra A. 1994. Use of the tetracycline promoter for the tightly regulated production of a murine antibody fragment in Escherichia coli. Gene 151:131-135.
41. Söding J. 2005. Protein homology detection by HMM-HMM comparison. Bioinformatics 21:951-960.
42. Söding J, Biegert A, Lupas AN. 2005. The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res 33:W244-W248.
43. Sogabe S, Yoshizumi A, Fukami TA, Shiratori Y, Shimizu S, Takagi H, Nakamori S, Wada M. 2003. The crystal structure and stereospecificity of levodione reductase from Corynebacterium aquaticum M-13. J Biol Chem 278:19387-19395.
44. Studier FW, Daegelen P, Lenski RE, Maslov S, Kim JF. 2009. Understanding the differences between genome sequences of Escherichia coli B strains REL606 and BL21(DE3) and comparison of the E. coli B and K-12 genomes. J Mol Biol 394:653-680.
45. Tanaka N, Nonaka T, Nakanishi M, Deyashiki Y, Hara A, Mitsui Y. 1996. Crystal structure of the ternary complex of mouse lung carbonyl reductase at 1.8Å resolution: The structural origin of coenzyme specificity in the short-chain dehydrogenase/reductase family. Structure 4:33-45.
46. Thoden JB, Wohlers TM, Fridovich-Keil JL, Holden HM. 2000. Crystallographic evidence for Tyr 157 functioning as the active site base in human UDP-galactose 4-epimerase. Biochemistry 39:5691-5701.
47. Tietze S, Apostolakis J. 2007. GlamDock: Development and validation of a new docking tool on several thousand protein-ligand complexes. J Chem Inf Model 47:1657-1672.
48. Wang W, Nema S, Teagarden D. 2010. Protein aggregation-Pathways and influencing factors. Int J Pharm 390:89-99.
49. Wierenga RK, Demaeyer MCH, Hol WGJ. 1985. Interaction of pyrophosphate moieties with α-helixes in dinucleotide binding-proteins. Biochemistry 24:1346-1357.
50. + and pseudotropine at 1.9Å resolution: Implication for stereospecific substrate binding and catalysis. Biochemistry 38:7630-7637.
51. Yaoi T, Miyazaki K, Oshima T, Komukai Y, Go M. 1996. Conversion of the coenzyme specificity of isocitrate dehydrogenase by module replacement. J Biochem 119:1014-1018.
52. Zhang L, Ahvazi B, Szittner R, Vrielink A, Meighen E. 1999. Change of nucleotide specificity and enhancement of catalytic efficiency in single point mutants of Vibrio harveyi aldehyde dehydrogenase. Biochemistry 38:11440-11447.